Identification of parasite-responsive cysteine proteases in Manduca sexta

Biological Chemistry

Volumn 390, Issue 5-6, 2009, Pages 493-502

  Serbielle, Céline ^a,c   Moreau, Sébastien ^a   Veillard, Florian ^a   Voldoire, Emilien ^a   Bézier, Annie ^a   Mannucci, Marie Anne ^b   Volkoff, Anne Nathalie ^b   Drezen, Jean Michel ^a   Lalmanach, Gilles ^a   Huguet, Elisabeth ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b UNIV MONTPELLIER   (France)

^c CNRS   (France)

Author keywords

Bracovirus; Cathepsin; Cystatin; Insect; Parasitoid wasp; Polydnavirus

Indexed keywords

CATHEPSIN B; CATHEPSIN L; COMPLEMENTARY DNA; CYSTATIN; CYSTEINE PROTEINASE; CYSTEINE PROTEINASE C1A; CYSTEINE PROTEINASE MSCATH1; CYSTEINE PROTEINASE MSCATH2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; COTESIA CONGREGATA; DNA DETERMINATION; ENZYME ISOLATION; ENZYME REGULATION; GENE EXPRESSION REGULATION; HEMOLYMPH; HOST PARASITE INTERACTION; IN VIVO STUDY; MANDUCA SEXTA; NONHUMAN; PARASITE VIRULENCE; PARASITISM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SYMBIONT; TRANSCRIPTION REGULATION; VIRUS GENE; WASP; WESTERN BLOTTING;

ANIMALS; CYSTATINS; CYSTEINE ENDOPEPTIDASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOST-PARASITE INTERACTIONS; INSECT PROTEINS; LARVA; MANDUCA; POLYDNAVIRIDAE; WASPS;

BRACOVIRUS; COTESIA CONGREGATA; HEXAPODA; MANDUCA SEXTA;

EID: 67649584023     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2009.061     Document Type: Article

References (48)

1. Abrahamson, M., Alvarez-Fernandez, M., and Nathanson, C.-M. (2003). Cystatins. Biochem. Soc. 70, 179-199.
2. Arai, S., Matsumoto, I., Emori, Y., and Abe, K. (2002). Plant seed cystatins and their target enzymes of endogenous and exogenous origin. J. Agric. Food Chem. 50, 6612-6617.
3. Attardo, G.M., Strickler-Dinglasan, P., Perkin, S.A.H., Caler, E., Bonaldo, M.F., Soares, M.B., El-Sayeed, N., and Aksoy, S. (2006). Analysis of fat body transcriptome from the adult tsetse fly, Glossina morsitans morsitans. Insect Mol. Biol. 15, 411-424.
4. Beckage, N.E., Tan, F.T., Schleifer, K.W., Lane, R.D., and Cherubin, L.L. (1994). Characterization and biological effects of Cotesia congregata Polydnavirus on host larvae of the tobacco hornworm, Manduca sexta. Arch. Insect Biochem. Phy-siol. 26, 165-195.
5. Brix, K., Dunkhorst, A., Mayer, K., and Jordans, S. (2008). Cysteine cathepsins: cellular roadmap to different functions. Biochimie 90, 194-207.
6. Cho, W.-L., Tsao, S.-M., Hays, A.R., Walter, R., Chen, J.-S., Snigirevskaya, E.S., and Raikhel, A.S. (1999). Mosquito cathepsin B-like protease involved in embryonic degradation of vitellin is produced as a latent extraovarian precursor. J. Biol. Chem. 274, 13311-13321.
7. Cygler, M., Sivaraman, J., Grochulski, P., Coulombe, R., Storer, A.C., and Mort, J.S. (1996). Structure of rat procathepsin B: model for inhibition of cysteine protease activity by the proregion. Structure 15, 405-416.
8. De Gregorio, E., Spellman, P.T., Rubin, G.M., and Lemaitre, B. (2001). Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA 98, 12590-12595.
9. Desjardins, C., Gundersen-Rindal, D., Hostetler, J., Tallon, L.J., Fuester, R.W., Schatz, M.C., Pedroni, M.J., Fadrosh, D.W., Haas, B.J., Toms, B.S., et al. (2007). Structure and evolution of a proviral locus of Glyptapanteles indiensis bracovirus. BMC Microbiol. 7, 61.
10. Desjardins, C., Gundersen-Rindal, D., Hostetler, J., Tallon, L.J., Fadrosh, D.W., Fuester, R.W., Pedroni, M.J., Haas, B.J., Schatz, M.C., Jones, K.M., et al. (2008). Comparative genomics of mutualistic viruses of Glyptapanteles parasitic wasps. Genome Biol. 9, R138.
11. Dickinson, D.P. (2002). Cysteine peptidases of mammals; their biological roles and potential effects in the oral cavity and other tissues in health and disease. Crit. Rev. Oral Biol. Med. 13, 238-275.
12. Espagne, E., Dupuy, C., Huguet, E., Cattolico, L., Provost, B., Martins, N., Poirie, M., Periquet, G., and Drezen, J.M. (2004). Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 306, 286-289.
13. Espagne, E., Douris, V., Lalmanach, G., Provost, B., Cattolico, L., Lesobre, J., Kurata, S., Iatrou, K., Drezen, J.M., and Huguet, E. (2005). A virus essential for insect host-parasite interactions encodes cystatins. J. Virol. 79, 9765-9776.
14. Fujimoto, Y., Kobayashi, A., Kurata, S., and Natori, S. (1999). Two subunits of the insect 26/29-kDa proteinase are probably derived from a common precursor protein. J. Biochem. (Tokyo) 125, 566-573.
15. Gregory, W.F. and Maizels, R.M. (2008). Cystatins from filarial parasites: evolution, adaptation and function in the host-parasite relationship. Int. J. Biochem. Cell Biol. 40, 1389-1398.
16. Harrison, R.L. and Bonning, B.C. (2001). Use of proteases to improve the insecticidal activity of baculoviruses. Biol. Control 20, 199-209.
17. Harwood, S.H., Grosovsky, A.J., Cowles, E.A., Davis, J.W., and Beckage, N.E. (1994). An abundantly expressed hemolymph glycoprotein isolated from newly parasitized Manduca sexta larvae is a polydnavirus gene product. Virology 205, 381-392.
18. Hegedus, D., O'Grady, M., Chamankhah, M., Baldwin, D., Gleddie, S., Braun, L., and Erlandson, M. (2002). Changes in cysteine protease activity and localization during midgut metamorphosis in the crucifer root maggot (Delia radicum). Insect Biochem. Mol. Biol. 32, 1585-1596.
19. Homma, K., Kurata, S., and Natori, S. (1994). Purification, characterization, and cDNA cloning of procathepsin L from the culture medium of NIH-Sape-4, an embryonic cell line of Sarcophaga peregrina (flesh fly), and its involvement in the differentiation of imaginal discs. J. Biol. Chem. 269, 15258-15264.
20. Karrer, K.M., Peiffer, S.L., and DiTomas, M.E. (1993). Two distinct gene subfamilies within the family of cysteine protease genes. Proc. Natl. Acad. Sci. USA 90, 3063-3067.
21. Koo, Y.D., Ahn, J.E., Salzman, R.A., Moon, J., Chi, Y.H., Yun, D.J., Lee, S.Y., Koiwa, H., and Zhu-Salzman, K. (2008). Functional expression of an insect cathepsin B-like counter-defence protein. Insect Mol. Biol. 17, 235-245.
22. Krupa, J.C., Hasnain, S., Nä gler, D.K., Ménard, R., and Mort, J.S. (2002). S2' substrate specificity and the role of His110 and His111 in the exopeptidase activity of human cathepsin B. Biochem. J. 361, 613-619.
23. Kurata, S., Saito, H., and Natori, S. (1992). Purification of a 29-kDa hemocyte proteinase of Sarcophaga peregrina. Eur. J. Biochem. 204, 911-914.
24. Lapointe, R., Tanaka, K., Barney, W.E., Whitfield, J.B., Banks, J.C., Béliveau, C., Stoltz, D., Webb, B., and Cusson, M. (2007). Genomic and morphological features of a banchine polydnavirus: comparison with bracovirus and ichnovirus. J. Virol. 81, 6491-6501.
25. Lecaille, F., Kaleta, J., and Brömme, D. (2002). Human and parasitic papain-like cysteine proteases: their role in physiology and pathology and recent developments in inhibitor design. Chem. Rev. 102, 4459-4488.
26. Levy, F., Rabel, D., Charlet, M., Bulet, P., Hoffmann, J.A., and Ehret-Sabatier, L. (2004). Peptidomic and proteomic analyses of the systemic immune response of Drosophila. Biochimie 86, 607-616.
27. Li, H., Tang, H., Sivakumar, S., Philip, J., Harrison, R.L., Gatehouse, J.A., and Bonning, B. (2008). Insectividal activity of a basement membrane-degrading protease against Heliothis virescens (Fabricius) and Acyrthosiphon pisum (Harris). J. Insect Physiol. 54, 777-789.
28. Liu, J., Shi, G.P., Zhang, W.Q., Zhang, G.R., and Xu, W.H. (2006). Cathepsin L function in insect moulting: molecular cloning and functional analysis in cotton bollworm, Helicoverpa armigera. Insect Mol. Biol. 15, 823-834.
29. Maizels, R.M., Blaxter, M.L., and Scott, A.L. (2001). Immunological genomics of Brugia malayi: filarial genes implicated in immune evasion and protective immunity. Parasite Immunol. 23, 327-344.
30. Miyaji, T., Kouzuma, Y., Yaguchi, J., Matsumoto, R., Kanost, M.R., Kramer, K.J., and Yonekura, M. (2007). Purification of a cysteine protease inhibitor from larval hemolymph of the tobacco hornworm (Manduca sexta) and functional expression of the recombinant protein. Insect Biochem. Mol. Biol. 37, 960-968.
31. Musil, D., Zucic, D., Turk, D., Engh, R.A., Mayr, I., Huber, R., Popovic, T., Turk, V., Towatari, T., Katunuma, N., et al. (1991). The refined 2.15 Å X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J. 10, 2321-2330.
32. Nègre, V., Hôtelier, T., Volkoff, A.-N., Gimenez, S., Cousserans, F., Mita, K., Sabau, X., Rocher, J., López-Ferber, M., d'Alen-çon, E., et al. (2006). SPODOBASE: an EST database for the lepidopteran crop pest Spodoptera. BMC Bioinform. 7, 322.
33. Nusawardani, T., Ruberson, J.R., Obrycki, J.J., and Bonning, B. (2005). Effects of a protease-expressing recombinant baculovirus insecticide on the parasitoid Cotesia marginiventris (Cresson). Biol. Control 35, 46-54.
34. Papanicolaou, A., Gebauer-Jung, S., Blaxter, M.L., McMilla, W.O., and Jiggins, C.D. (2008). Butterflybase: a platform for lepidopteran genomics. Nucleic Acids Res. 36, D582-D587.
35. Provost, B., Varricchio, P., Arana, E., Espagne, E., Falabella, P., Huguet, E., La Scaleia, R., Cattolico, L., Poirié, M., Malva, C., et al. (2004). Bracoviruses contain a large multigene family coding for protein tyrosine phosphatases. J. Virol. 78, 13090-13103.
36. Rodriguez-Pérez, M.A., Dumpit, R.F., Lenz, J.M., Powell, E.N., Tam, S.Y., and Beckage, N.E. (2005). Host refractoriness of the tobacco hornworm, Manduca sexta, to the braconid endoparasitoid Cotesia flavipes. Arch. Insect Biochem. Physiol. 60, 159-171.
37. Saito, H., Kurata, S., and Natori, S. (1992). Purification and characterization of a hemocyte proteinase of Sarcophaga, possibly participating in elimination of foreign substances. Eur. J. Biochem. 209, 939-944.
38. Schierack, P., Lucius, R., Sonnenburg, B., Schilling, K., and Hart-mann, S. (2003). Parasite-specific immunomodulatory functions of filarial cystatin. Infect. Immun. 71, 2422-2429.
39. Serbielle, C., Chowdhury, S., Pichon, S., Dupas, S., Lesobre, J., Purisima, E.O., Drezen, J.M., and Huguet, E. (2008). Viral cystatin evolution and three-dimensional structure modelling: a case of directional selection acting on a viral protein involved in a host-parasitoid interaction. BMC Biol. 6, 38.
40. Shindo, T. and Van Der Hoorn, R.A. (2008). Papain-like cysteine proteases: key players at molecular battlefields employed by both plants and their invaders. Mol. Plant Pathol. 9, 119-125.
41. Song, K.-H., Jung, M.-K., Eum, J.-H., Hwang, I.-C., and Han, S. S. (2008). Proteomic analysis of parasitized Plutella xylostella larvae plasma. J. Insect Physiol. 54, 1271-1280.
42. Tanaka, K., Lapointe, R., Barney, W.E., Makkay, A.M., Stoltz, D., Cusson, M., and Webb, B.A. (2007). Shared and species-specific features among ichnovirus genomes. Virology 363, 26-35.
43. Tang, H., Li, H., Meng Lei, S., Harrison, R.L., and Bonning, B.C. (2007). Tissue specificity of a baculovirus-expressed, basement membrane-degrading protease in larvae of Heliothis virescens. Tissue Cell 39, 431-443.
44. Turk, B., Turk, V., and Turk, D. (1997). Structural and functional aspects of papain-like cysteine proteinases and their protein inhibitors. Biol. Chem. 378, 141-150.
45. Turnbull, M. and Webb, B. (2002). Perspectives on polydnavirus origins and evolution. Adv. Virus Res. 58, 203-254.
46. Uchida, K., Ohmori, D., Ueno, T., Nishizuka, M., Eshita, Y., Fukunaga, A., and Kominami, E. (2001). Preoviposition activation of cathepsin-like proteinases in degenerating ovarian follicles of the mosquito Culex pipiens pallens. Dev. Biol. 237, 68-78.
47. Webb, B.A., Strand, M.R., Dickey, S.E., Beck, M.H., Hilgarth, R.S., Barney, W.E., Kadash, K., Kroemer, J.A., Lindstrom, K.G., Rattanadechakul, W., et al. (2006). Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 347, 160-174.
48. Yan, J., Cheng, Q., Li, C.B., and Aksoy, S. (2002). Molecular characterization of three gut genes from Glossina morsitans morsitans: cathepsin B, zinc-metalloprotease and zinccarboxypeptidase. Insect Mol. Biol. 11, 57-65.